Skip to main content

Advertisement

SpringerLink
Log in

Fine scale population structure of dugongs (Dugong dugon) implies low gene flow along the southern Queensland coastline

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Populations of marine mammals can show the signature of phylogeographical breaks and restricted connectivity despite the apparent lack of physical boundaries in the marine environment and their high dispersal abilities. Dugongs (Dugong dugon) do not appear to undertake regular migrations but may show localised movement related to water temperature or seagrass availability. Previous mitochondrial DNA studies suggested that despite a strong phylogeographic break in the Torres Strait, there is local panmixia in Australian waters. In this study, we conducted a comprehensive study of the four major dugong populations in southern Queensland. We analysed genotypes of 1,293 dugongs based on 24 microsatellite loci from the four major dugong locations in the region (from south to north): Moreton Bay, Great Sandy Straits, Hervey Bay and Shoalwater Bay. Diversity levels were similar across locations (observed heterozygosity 0.48–0.52, allelic richness 4.3–4.5). There was low but significant population differentiation in southern Queensland (FST ranged from 0.005 to 0.040 and Jost’s DEST ranged from 0.001 to 0.031 for microsatellite data). Bayesian clustering analysis implemented in STRUCTURE largely distinguished the southern Moreton Bay population from the three more northern populations. Twelve mitochondrial control region haplotypes identified from a subset of 182 samples confirmed significant population structuring (FST ranged from 0.16 to 0.28). These data suggested that the frequency and extent of dugong movements are insufficient to disrupt the long-term existence of at least two breeding populations in southern Queensland.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ansmann IC, Parra GJ, Lanyon JM, Seddon JM (2012) Fine-scale genetic population structure in a mobile marine mammal: inshore bottlenose dolphins in Moreton Bay, Australia. Mol Ecol 21:4472–4485

    Article  PubMed  Google Scholar 

  • Arraut E, Marmontel M, Mantovani J, Novo E, Macdonald D, Kenward R (2010) The lesser of two evils: seasonal migrations of Amazonian manatees in the Western Amazon. J Zool 2809:247–256

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • Bérubé M, Palsbøll P (1996) Identification of sex in Cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol 5:283–287

    Article  PubMed  Google Scholar 

  • Blair D, McMahon A, McDonald B, Tikel D, Waycott M, Marsh H (2013) Pleistocene sea level fluctuations and the phylogeography of the dugong in Australian waters. Mar Mamm Sci. doi:10.1111/mms.12022

    Google Scholar 

  • Bonde R (2009) Population Genetics and Conservation of the Florida Manatee: Past, present, and future. PhD thesis, University of Florida, Gainesville

  • Broderick D, Ovenden J, Slade R, Lanyon J (2007) Characterization of 26 new microsatellite loci in the dugong (Dugong dugon). Mol Ecol Notes 7:1275–1277

    Article  CAS  Google Scholar 

  • Burgess E, Brown J, Lanyon J (2013) Sex, scarring, and stress: understanding seasonal costs in a cryptic marine mammal. Conserv Physiol 1(1):cot014

    Google Scholar 

  • Cassens I, Van Waerebeek K, Best PB, Tzika A, Van Helden AL, Crespo EA, Milinkovitch MC (2005) Evidence for male dispersal along the coasts but no migration in pelagic waters in dusky dolphins (Lagenorhynchus obscurus). Mol Ecol 14:107–121

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Coles R, Grech A, Rasheed M, McKenzie L (2012) Evaluating risk to seagrasses in the Tropical Indo-Pacific Region. In: Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia

  • Cope R (2014) Animal movement between populations deduced from family trees: a test case on dugongs in southern Queensland. PhD thesis, The University of Queensland, St Lucia

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    Article  PubMed  Google Scholar 

  • Deutsch C, Reid JP, Bonde R, Easton D, Kochman H H, O’Shea T (2003) Seasonal movements, migratory behavior, and site fidelity of West Indian manatees along the Atlantic coast of the United States. Wildl Monogr 151:1–77

    Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillet BJ, Ovenden JR (2013) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14(1):209–214

    Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc R Soc B 264:127–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fontaine MC, Baird SJ, Piry S, Ray N, Tolley KA, Duke S, Birkun A Jr, Ferreira M, Jauniaux T, Llavona A, Ozturk B, Ozturk AA, Ridoux V, Rogan E, Sequeira M, Siebert U, Vikingsson GA, Bouquegneau JM, Michaux JR (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. BMC Biol 5:30

    Article  PubMed Central  PubMed  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Gales NJ, McCauley RD, Lanyon JM, Holley DK (2004) Change in abundance of dugongs in Shark Bay, Ningaloo and Exmouth Gulf, Western Australia: evidence for large scale migration. Wildl Res 31:283–290

    Article  Google Scholar 

  • Garcia-Rodriguez AI, Bowen BW, Domning D, Mignucci-Giannoni A, Marmontel M, Montoya-Ospina A, Morales-Vela B, Rudin M, Bonde RK, McGuire PM (1998) Phylogeography of the West Indian manatee (Trichechus manatus): how many populations and how many taxa? Mol Ecol 7:1137–1149

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. http://www.unil.ch/izea/softwares/fstat.html. Accessed 02 May 2013

  • Greenwood P (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Gupta S, Thangaraj K, Singh L (2006) A simple and inexpensive molecular method for sexing and identification of the forensic samples of elephant origin. J Forensic Sci 51:805–807

    Article  CAS  PubMed  Google Scholar 

  • Hagihara R, Jones R, Grech A, Lanyon J, Sheppard J, Marsh H (2013) Improving population estimates by quantifying diving and surfacing patterns: A dugong example. Mar Mamm Sci. doi:10.1111/mms.12041

    Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer, Sunderland

    Google Scholar 

  • Heinsohn G, Spain A (1974) Effects of a tropical cyclone on littoral and sub-littoral biotic communities and on a population of dugongs (Dugong dugon (Miiller)). Biol Conserv 6:143–152

    Article  Google Scholar 

  • Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Konovalov D, Manning C, Henshaw M (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782

    Article  Google Scholar 

  • Lanyon J (2003) Distribution and abundance of dugongs in Moreton Bay, Queensland, Australia. Wildl Res 30:397–409

    Article  Google Scholar 

  • Lanyon J, Sneath H, Kirkwood J, Slade R (2002) Establishing a mark-recapture program for dugongs in Moreton Bay, south-east Queensland. Austr Mammalogy 24:51–56

    Article  Google Scholar 

  • Lanyon J, Johns T, Sneath H (2005) Year round presence of dugongs in Pumicestone Passage, south-east Queensland, examined in relation to water temperature and seagrass distribution. Wildl Res 32:361–368

    Article  Google Scholar 

  • Lanyon J, Slade R, Sneath H, Broderick D, Kirkwood J, Limpus D, Limpus C, Jessop T (2006) A method for capturing dugongs (Dugong dugon) in open water. Aquat Mamm 32:196–201

    Article  Google Scholar 

  • Lanyon J, Sneath H, Slade R (2007) Mark-recapture analysis of dugong populations. In: 17th international Biennial conference on marine mammals, Cape Town, South Africa

  • Lanyon J, Sneath H, Long T (2010) Three skin sampling methods for molecular characterisation of free-ranging dugong (Dugong dugon) populations. Aquat Mamm 36:298–306

    Article  Google Scholar 

  • Lowther A, Harcourt R, Goldsworthy S, Stow A (2012) Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity. Anim Behav 83:691–701

    Article  Google Scholar 

  • Luikart G, Ryman N, Tallmon D, Schwartz M, Allendorf F (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Gen 11:255–373

    Article  Google Scholar 

  • Marsh H, Rathbun G (1990) Development and application of conventional and satellite radio-tracking techniques for studying dugong movements and habitat usage. Austr Wildl Res 17:83–100

    Article  Google Scholar 

  • Marsh H, Corkeron P, Lawler IR, Lanyon J, Preen AR (1996) The status of the dugong in the Southern Great Barrier Reef Marine Park. Great Barrier Reef Marine Park Authority Research Publication, Townsville 41

    Google Scholar 

  • Marsh H, De’ath G, Gribble N, Lane B (2001a) Shark control records hindcast serious decline in dugong numbers off the urban coast of Queensland. Great Barrier Reef Marine Park Authority, Research publications series no. 70, part 1

  • Marsh H, De’Ath G, Gribble N, Lane B, Lawler I (2001b) Dugong distribution and abundance in the southern Great Barrier Reef Marine Park and Hervey Bay: results of an aerial survey in October-December 1999. Great Barrier Reef Marine Park Authority, Research publications series no. 70, part 2

  • Marsh H, Penrose H, Eros C, Hughes J (2002) Dugong status report and action plans for countries and territories United Nations Environment Programme, Nairobi

  • Marsh H, De’Ath G, Gribble N, Lane B (2005) Historical marine population estimates: Triggers or targets for conservation? The dugong case study. Ecol Appl 15:481–492

    Article  Google Scholar 

  • Marsh H, O’Shea T, Reynolds J III (2012) Ecology and conservation of the Sirenia: Dugongs and manatees. Cambridge University Press, Cambridge

    Google Scholar 

  • McDonald B (2005) Population genetics of dugongs around Australia: Implications of gene flow and migration. PhD thesis, James Cook University, Townsville

  • McHale M, Broderick D, Ovenden JR, Lanyon JM (2008) A PCR assay for gender assignment in dugong (Dugong dugon) and West Indian manatee (Trichechus manatus). Mol Ecol Resour 8:669–670

    Article  CAS  PubMed  Google Scholar 

  • McKenzie L, Yoshida R, Grech A, Coles R (2010) Queensland seagrasses. Status 2010—Torres Strait and East Coast. Fisheries Queensland (DEEDI), Cairns

  • Meager J, Limpus C, Sumpton W (2013) A review of the population dynamics of dugongs in southern Queensland: 1830-2012. Department of Environment and Heritage Protection, Queensland Government, Brisbane

    Google Scholar 

  • Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated blood cells. Nucleic Acids Res 16:1215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morales-Vela B, Padilla-Saldivar J, Mignucci-Giannoni A (2003) Status of the Manatee (Trichechus manatus) along the Northern and Western Coasts of the Yucatan Peninsula, Mexico. Caribb J Sci 39:42–49

    Google Scholar 

  • Ovenden JR, Peel D, Street R, Courtney AJ, Hoyle SD, Peel SL, Podlich H (2007) The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol 16:127–138

    Article  CAS  PubMed  Google Scholar 

  • Palstra F, Fraser D (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2:2357–2365

    Article  PubMed Central  PubMed  Google Scholar 

  • Park S (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD thesis, University of Dublin, Dublin

  • Pause Tucker K, Hunter M, Bonde R, Austin J, Clark A, Beck C, McGuire P, Oli M (2012) Low genetic diversity and minimal population substructure in the endangered Florida manatee: implications for conservation. J Mamm 93:1504–1511

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peel D, Waples R, Macbeth G, Do C, Ovenden J (2013) Accounting for missing data in the estimation of contemporary genetic effective population size (Ne). Mol Ecol Res 13:243–253

    Article  CAS  Google Scholar 

  • Powell J, Kouadio A (2008) Trichechus senegalensis IUCN red list of threatened species. Version 2011.2. International Union for Conservation of Nature

  • Preen A (1992) Interactions between dugongs and seagrasses in a subtropical environment. PhD thesis, James Cook University, Townsville

  • Preen A, Marsh H (1995) Response of dugongs to large-scale loss of seagrass from Hervey Bay, Queensland, Australia. Wildl Res 22:507–519

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rizzo L, Schulte D (2009) A review of humpback whales’ migration patterns worldwide and their consequences to gene flow. J Mar Biol Assoc UK 89:995–1002

    Article  Google Scholar 

  • Rosel PE, France SC, Wang JY, Kocher TD (1999) Genetic structure of harbour porpoise Phocoena phocoena populations in the northwest Atlantic based on mitochondrial and nuclear markers. Mol Ecol 8:S41–S54

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Satizabal P, Mignucci-Giannoni AA, Duchene S, Caicedo-Herrera D, Perea-Sicchar CM, Garcia-Davila CR, Trujillo F, Caballero SJ (2012) Phylogeography and sex-biased dispersal across riverine manatee populations (Trichechus inunguis and Trichechus manatus) in South America. PLoS ONE 7:e52468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Sheppard J, Preen A, Marsh H, Lawler I, Whiting S, Jones R (2006) Movement heterogeneity of dugongs, Dugong dugon (Müller), over large spatial scales. J Exp Mar Biol Ecol 334:64–83

    Article  Google Scholar 

  • Sobtzick S, Hagihara R, Grech A, Marsh H (2012) Aerial survey of the urban coast of Queensland to evaluate the response of the dugong population to the widespread effects of the extreme weather events of the summer of 2010–2011. Australian Marine Mammal Centre and the National Environmental Research Program

  • Sprogis KR (2008) Small-scale habitat use and movements of dugongs (Dugong dugon) with respect to tides, foraging time and vessel traffic on the eastern banks of Moreton Bay. Honours thesis, University of Queensland, St Lucia

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Taylor H, Rasheed M (2010) Torres Strait Dugong Sanctuary seagrass baseline survey. Fisheries Queensland (DEEDI), Cairns

  • Tikel D (1997) Using a genetic approach to optimise dugong (Dugong dugon) conservation management. PhD thesis, James Cook University, Townsville

  • Van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waples R, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resources 8:753–756

    Article  Google Scholar 

  • Waples R, Luikart G, Faulkner J, Tallmon D (2013) Simple life history traits explain key effective population size ratios across diverse taxa. Proc R Soc B. doi:10.1098/rspb.2013.1339

    PubMed Central  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wiszniewski J, Beheregaray LB, Allen S, Möller L (2010) Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in Southeastern Australia. Conserv Genet 11:1405–1419

    Article  Google Scholar 

Download references

Acknowledgments

Order of authorship follows the ‘first-last-then others’ convention. Thanks to The University of Queensland Dugong Research Team, particularly Rob Slade, Erin Neal, Ben Schemel, Liz Burgess, Paul Sprecher, Merrick Ekins and Gio Damiani for assistance in the field. Thanks also to those involved in laboratory analyses, including Brenda McDonald, Julie Macaranas, Deanne Waine and Sean Corley. Thanks to Frank Loban (Torres Strait Regional Authority), and to Terrence Whap and the Mabuiag Island Community for dugong tissue samples. This research was funded by an Australian Research Council (ARC) Linkage Grant with industry partners Sea World Australia and Sibelco (formerly Unimin and Consolidated Rutile Ltd) and the Winifred Violet Scott Foundation and Australian Marine Mammal Centre. Sea World Research and Rescue Foundation Australia (and Trevor Long) provided generous in-kind support for the sampling trips to the Great Sandy Straits. Dugongs were sampled under The University of Queensland Animal Ethics Permits #ZOO/ENT/344/04/NSF/CRL to #SBS/290/11/ARC/CRL/SEAWORLD/ACAMMS/AMMC, Scientific Purposes Permits #WISP01660304, WISP03294105, WISP04937308, and WISP07255110 to WISP12255110, Moreton Bay Marine Parks Permits #QS2000 to #QS2010CV L228, Great Sandy Marine Parks Permit QS2010-GS043 and Great Barrier Reef Marine Park Permit #G07 = 23274:1.

Author information

Authors and Affiliations

  1. School of Veterinary Science, The University of Queensland, Gatton, QLD, 4343, Australia

    Jennifer M. Seddon & Christine L. Dudgeon

  2. Molecular Fisheries Laboratory, School of Biomedical Sciences, The University of Queensland, St Lucia, QLD, 4072, Australia

    Jennifer R. Ovenden, Damien Broderick & Christine L. Dudgeon

  3. Marine Vertebrate Ecology Research Group, School of Biological Sciences, The University of Queensland, St Lucia, QLD, 4072, Australia

    Helen L. Sneath & Janet M. Lanyon

Authors
  1. Jennifer M. Seddon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer R. Ovenden
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helen L. Sneath
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Damien Broderick
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christine L. Dudgeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Janet M. Lanyon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer M. Seddon.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 50 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seddon, J.M., Ovenden, J.R., Sneath, H.L. et al. Fine scale population structure of dugongs (Dugong dugon) implies low gene flow along the southern Queensland coastline. Conserv Genet 15, 1381–1392 (2014). https://doi.org/10.1007/s10592-014-0624-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0624-x

Keywords

Search

Navigation